Distribution of pair quality in a tree-nestingwaterbird colony: central-periphery model vs.satellite model

Piotr Minias, Krzysztof Kaczmarek, and Tomasz Janiszewski

Abstract: The spatial distribution of pair quality within waterbird colonies has been suggested to follow one of three theo-retical models: central-periphery, satellite, or random. The central-periphery pattern occurs in homogeneous habitats, wheregood-quality pairs occupy better protected, central nesting sites. In contrast, the satellite and random patterns are associatedwith heterogeneous habitats and they assume that good-quality pairs occupy the most attractive nesting sites irrespectivelyof their location within the colony. Spatial patterns of laying date, clutch size, and fledging success were analysed with geo-statistical tools in the colony of tree-nesting subspecies of Great Cormorant (Phalacrocorax carbo sinensis (Blumenbach,1798)) in central Poland. There was support for the random or satellite model in the distribution of clutch size, which wasconsidered a reliable proxy of pair quality. We also found a positive correlation of clutch size with nest height. These resultsimplicate that the habitat of tree-nesting colonial waterbirds may produce sufficient variation in the nesting-site quality todisrupt the central-periphery gradients of pair-quality distribution. In contrast, distribution of fledging success within the col-ony followed a clear central-periphery pattern, which was suggested to reflect an increased predation rate at the edges of thecolony, rather than the intrinsic quality of breeding birds.

Key words: central-periphery, coloniality, Great Cormorant, Phalacrocorax carbo sinensis, spatial autocorrelation.

Résumé : Il a été proposé que la répartition spatiale de la qualité des couples au sein de colonies d’oiseaux aquatiques seconformait à l’un ou l’autre des trois modèles théoriques suivants : centre-périphérie, satellite et aléatoire. La distributioncentre-périphérie est observée dans les habitats homogènes, où les couples de bonne qualité occupent des sites de nidifica-tion centraux relativement bien protégés. En revanche, les distributions de types satellite et al.éatoire sont associées à des ha-bitats hétérogènes et découlent du fait que les couples de bonne qualité occupent les sites de nidification les plus attrayants,quelque soit leur emplacement au sein de la colonie. Les patrons de distribution spatiale de la date de la ponte, de la tailledes nichées et du succès d’envol ont été analysés à l’aide d’outils géostatistiques dans une colonie d’une sous-espèce arbori-cole de grands cormorans (Phalacrocorax carbo sinensis (Blumenbach, 1798)) du centre de la Pologne. La distribution dela taille des nichées, considérée comme une variable substitutive fiable de la qualité des couples, indiquait un modèle detype aléatoire ou satellite. Nous avons également relevé une corrélation positive entre la taille des nichées et la hauteur dunid. Ces résultats indiquent que l’habitat d’oiseaux aquatiques coloniaux arboricoles peut présenter des variations de la qua-lité des sites de nidification suffisamment importantes pour perturber une distribution centre-périphérie de la qualité descouples. En revanche, la distribution du succès d’envol au sein de la colonie suivait un patron centre-périphérie très net, cequi reflèterait un taux de prédation accru en bordure de la colonie, plutôt que la qualité intrinsèque des couples nicheurs.

Mots‐clés : centre-périphérie, colonialité, grand cormoran, Phalacrocorax carbo sinensis, autocorrélation spatiale.

[Traduit par la Rédaction]

Introduction

Spatial distribution of pair quality within avian coloniesmay depend on both behavioural and environmental traits(Velando and Freire 2001). Heterogeneity of habitat is con-sidered one of primary factors affecting patterns of colonyformation and pair-quality distribution. In homogeneous hab-itats central parts of the colonies offer the highest benefits interms of fitness owing to the effectiveness of group defence,which decreases from centres towards the edges (Götmark

and Andersson 1984; Yorio and Quintana 1997). In conse-quence, central breeding pairs are likely to achieve higherbreeding success owing to decreased predation-related lossesof eggs and chicks. Since pairs of high intrinsic quality (ex-pressed by age, social status, or physical condition) are ableto win the competition for attractive central sites and relegatepoor-quality conspecifics to the edges of developing colony(Porter 1990), a central-periphery gradient of pair quality islikely to occur. Central-periphery distribution of pair qualitywas found in several waterbird species, mainly larids, which

Received 26 December 2011. Accepted 5 May 2012. Published at www.nrcresearchpress.com/cjz on 23 June 2012.

P. Minias and T. Janiszewski. Department of Teacher Training and Biodiversity Studies, University of Łódź, Banacha 1/3, 90-237 Łódź,Poland.K. Kaczmarek. Medical University of Łódź, Sterlinga 1/3, 91-425 Łódź, Poland.

Corresponding author: Piotr Minias (e-mail: pminias@op.pl).

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Can. J. Zool. 90: 861–867 (2012) doi:10.1139/Z2012-054 Published by NRC Research Press

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typically breed in highly homogeneous habitats. Higherfledging success of individuals breeding in higher densitiesor in the centres of colonies was recorded, among others, inBlack-headed Gull (Chroicocephalus ridibundus (L., 1766))(Patterson 1965), Black-legged Kittiwake (Rissa tridactyla(L., 1758)) (Coulson 1968), Ring-billed Gull (Larus delawar-ensis Ord, 1815) (Dexheimer and Southern 1974), and Cas-pian Tern (Hydroprogne caspia (Pallas, 1770)) (Antolos etal. 2006). Similar patterns were found in chick survival ofCommon Tern (Sterna hirundo L., 1758) (Becker 1995) andHerring Gull (Larus argentatus Pontoppidan, 1763) (Savocaet al. 2011). Higher reproductive success in the areas of highnest density was found also in the colonies of tree-nestingwaterbirds, e.g., Cattle Egret (Bubulcus ibis (L., 1758)) (Ran-glack et al. 1991).In contrast, heterogeneous habitats provide considerable

variation in the physical quality of nesting sites, which maybe independent of the location within the colony.High-quality pairs are able to occupy the best available nestsites and the choice of weaker conspecifics is consequentlylimited to less attractive nesting places. If nesting in good-quality sites is associated with high benefits in terms of fit-ness, the distribution of pair quality within a colony shouldcorrespond to the distribution of nesting-site quality. Assum-ing a random distribution of good-quality nesting sites withina colony, the spatial patterns of pair quality could be consis-tently random, or alternatively may follow a satellite model.The theoretical satellite model occurs when poor-quality indi-viduals are attracted to nest around the high-quality pair. Thebenefits from clustering close to the pairs of high quality in-clude achieving extra-pair copulations by poor-quality fe-males (Wagner et al. 1996) and acquisition of better site ormate in the following years (Aebischer et al. 1995). Supportfor the satellite model was found in European Shag (Phala-crocorax aristotelis (L., 1761)) (Velando and Freire 2001), aspecies that nests in ground and rock cavities of varying anti-predator safety.There is a lack of detailed spatial analyses of breeding pa-

rameters in tree-nesting colonial waterbirds. In large avianspecies exploiting forest-like habitats, physical quality ofnest sites is likely to be primarily determined by the heightand diameter of potential nesting trees, which affect accessi-bility of nests for ground or tree-dwelling predators and neststability (Post 1990; Ranglack et al. 1991). We hypothesizethat forest-like habitats may provide sufficient variation innesting-site quality to disrupt central-periphery distributionof pair quality in colonial waterbirds. In consequence, weexpect basic breeding parameters to follow the satellite orrandom distribution, as it could be more beneficial for agood-quality breeding pair to occupy a good-quality nestingsite irrespectively of its location within the colony, likewisein the central and peripheral zones. To verify the hypothesis,we tested the assumptions of three theoretical distributions(central-periphery, satellite, and random) for basic breedingparameters (laying date, clutch size, and fledging success) oftree-nesting subspecies of Great Cormorant (Phalacrocoraxcarbo sinensis (Blumenbach, 1798)). For that purpose, weapplied the techniques of geostatistical analysis presented byRossi et al. (1992), which describe the degree of spatial de-pendence of the data by relating the values of reproductiveparameters of each breeding pair to the parameters of neigh-

bouring pairs located in varying distances, i.e., within thelags of different radii. According to the theory developed byVelando and Freire (2001), the central-periphery model as-sumes that variation in pair quality (measured by semi-variance) shows low values at short distances (lags) andincreases with increasing lag, as pairs of certain-qualityneighbour with similar-quality pairs (Fig. 1a). For this rea-son, the model also assumes positive spatial autocorrelationat short lags. In the satellite model, semivariance is high atshort lags, as there is considerable variation in the quality ofneighbouring pairs and then decreases rapidly to reach a con-stant value at medium and long lags (Fig. 1b). A negativeautocorrelation at short lags is expected in this model. Incontrast, the random distribution is characterized by constantlevel of semivariance at all lags (Fig. 1c) and a lack of auto-correlation.

Materials and methodsSpatial patterns of breeding parameters were investigated

in 2004 in the Great Cormorant colony at the Jeziorsko reser-voir, central Poland. The colony was located near Mikołaje-wice village (51°43′N, 18°38′E), in the area covered withwillow shrubs dominated by white willow (Salix alba L.)and large grey willow (Salix cinerea L.). The colony was vis-ited in 5-day intervals from the onset of breeding activities inmid-March to the end of the breeding season in mid-July.During the entire breeding season, we recorded 381 activenests in the colony. All the nests were individually marked.During the visits, we performed regular checks of nests to es-timate date of laying of the first egg (assigned to 10-day in-tervals, starting from 21 March), clutch size, and fledgingsuccess (number of fledged chicks). We recorded laying datein 178 (median between 31 March and 1 April), clutch sizein 299 (3.91 ± 0.05, mean ± SE), and fledging success in293 (2.18 ± 0.08, mean ± SE) randomly distributed nests.All the nests within the colony were mapped with hand-

held global positioning system (GPS) unit (Garmin GpsMap60Cx; Garmin, Olathe, Kansas, USA) with European Geo-stationary Navigation Overlay Service (EGNOS) ensuring ac-curacy of 1–1.5 m. Nest coordinates were used to calculatedistances between all the nests. Based on the nest distancematrix, we calculated two characteristics of nest location:nest density (number of nests within the radius of 10 m) anddistance to the centre of the colony (m). The nest density was21.00 ± 0.83 nests (mean ± SE) per 10 m radius and the dis-tance to the colony centre was 70.39 ± 1.49 m (mean ± SE).Both characteristics of nest location were negatively corre-lated, as higher nesting densities were recorded in the centralparts of the colony (r = –0.36, N = 381, P < 0.001). Thecentre of the colony was calculated as the mean coordinatesof all the nests within the colony. Characteristics of nest loca-tion were calculated for all the nests recorded in the colonythroughout the breeding season, as there was no time gap be-tween the breeding activities of the earliest and the latest pairs.We also recorded nest height from the ground to the bottom ofthe nest with precision of 0.5 m for a random sample of 180nests. The nest height was 4.71 ± 0.12 m (mean ± SE).Spatial distribution of breeding parameters was analyzed

with variograms presenting semivariance values bgðhÞ for allchosen lags, according to the following equation:

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bgðhÞ ¼ 1

2NðhÞXNðhÞi¼1

½zðxiÞ � zðxi þ hÞ�2

To verify the satellite model, which assumes a rapid decreaseof semivariance over small lags, we presented small-scalevariograms in which lags were set to 6 m with the toleranceof 3 m. The length of lag (6 m) was chosen to producesufficiently large sample size of pair comparisons, especiallyin the first lag. To test the assumptions of central-peripheryand random models, we calculated large-scale variograms inwhich lags were set to 10 m with the tolerance of 5 m.Small-scale variograms were calculated for three lags from0 to 15 m (lag upper limits set to 3, 9, 15 m) and large-scale variograms for nine lags from 0 to 85 m (lag upperlimits set to 5, 15, 25, …, 85 m). All the variograms werecalculated using the geostatistical software VARIOWIN(Pannatier 1996).Spatial autocorrelations of laying date, clutch size, and

fledging success were tested with Pearson product momentcorrelation according to the following equation:

rðhÞ ¼ 1

NðhÞ

XNðhÞi¼1

½zðxiÞ � mx�½zðxi þ hÞ � mxþh�SxSxþh

where r(h) is a product–moment correlation coefficient esti-mated for lag h; N(h) is a number of pairs of nests separatedby lag h; z(xi) and z(xi + h) are the values of the variable re-corded for the pair i of nests separated by lag h; mx and Sxare, respectively, mean value and standard deviation calcu-lated for all z(xi); mx+h and Sx+h are, respectively, mean valueand standard deviation calculated for all z(xi + h).The spatial autocorrelations were calculated for the first

lag of the small-scale variogram analysis (0–3 m).The relationships between breeding parameters (laying

date, clutch size, and fledging success) and particular charac-teristics of nest location (nest density, distance to the colonycentre) were checked with the Pearson correlation. To ac-count for the variation in nest location, we used a multipleregression analysis while investigating the relationships be-tween nest height and particular breeding parameters. Thestepwise procedures of backward removal were used to select

Fig. 1. Three within-colony theoretical distributions of pair quality: central-periphery (a), satellite (b), and random (c). Spatial distribution areshown on the left; solid circles represent high-quality pairs and open circles represent low-quality pairs. Variograms for each model are shownon the right. Semivariances are shown in each lag, with high values indicating negative autocorrelation and low values indicating a positiveautocorrelation. Figure adapted from Velando and Freire (2001) and reproduce with permission of Condor, vol. 103, issue 3, p. 547, CooperOrnithological Society ©2001.

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for significant independent variables. Prior to analysis, nestheight was log-transformed to improve normality. The esti-mate coefficients (b ± SE) were used to assess the strengthof independent factor on the dependent variable. The differ-ences between slope coefficients of regression lines weretested with the analysis of covariance (ANCOVA). All statis-tics followed Zar (1996).

Results

We found that laying date correlated negatively with nestdensity (r = –0.23, N = 178, P = 0.002) and positively withdistance to the colony centre (r = 0.17, N = 178, P = 0.020).These relationships indicated central-periphery pattern of col-ony formation, with early breeders occupying nesting sites inthe central parts of the colony and late-breeding pairs occu-pying edge sites. Both clutch size and fledging success werepositively related with nest density (r = 0.13, N = 299, P =0.020 and r = 0.25, N = 293, P = 0.023, respectively), andthe relationship was stronger for the fledging success(ANCOVA—clutch size: b ± SE = 0.008 ± 0.003; fledgingsuccess: b ± SE = 0.021 ± 0.005; F[1,589] = 317.31, P <0.001). There was no relationship between clutch size andthe distance to the colony centre (r = –0.07, N = 299, P =0.26), which suggested that the spatial distribution of pairquality did not follow the central-periphery gradient. Therewas a negative relationship between fledging success and dis-tance to the colony centre (r = –0.12, N = 293, P = 0.046).The multiple regression analysis indicated that after account-ing for nest density, there was a significant relationship be-tween clutch size and nest height (F[1,151] = 3.91, P =0.049). We found that Great Cormorants occupying nests lo-cated high off the ground laid bigger clutches (b ± SE =0.41 ± 0.20). There was no relationship between nest heightand laying date (F[1,91] = 0.07, P = 0.78) or between nestheight and fledging success (F[1,151] = 1.92, P = 0.17).There was no support for the satellite model of colony for-

mation in the small-scale variogram of laying date (Fig. 2a).We found a significant positive autocorrelation in the first lag(r = 0.22, N = 160, P = 0.005), which suggestedcentral-periphery model of colony formation. This was con-firmed by a large-scale variogram analysis, which showed aconstant increase in semivariance with increasing lag(Fig. 3a). Semivariance increased 1.47-fold over the first sixlags (0–55 m) and then stabilized. A small-scale variogramof clutch size suggested the satellite model of pair-qualitydistribution within the colony, as there was a slight decreasein the semivariance over the first three lags (Fig. 2b). The au-tocorrelation coefficient for the first lag was negative, but therelationship was not significant (r = –0.03, N = 314, P =0.67). Large-scale variogram of clutch size indicated a ran-dom distribution of pair quality within the colony, as therewas no directional trend of semivariance over all chosen lags(Fig. 3b). Distribution of fledging success within the colonywas confirmed to follow a central-periphery model. Therewas a positive autocorrelation of fledging success in the firstlag (r = 0.19, N = 314, P < 0.001). Small-scale variogramdid not support the satellite model (Fig. 2c) and there was aconstant increase in semivariance over all lags in the large-scale variogram analysis (Fig. 3c).

DiscussionGeostatistical analysis of laying date supported the central-

periphery pattern of colony formation in the Great Cormor-ant. According to this model, the central nesting sites wereoccupied earlier compared with the peripheral sites, whichsuggested higher quality of the central breeding pairs. Incontrast, distribution of clutch size within the studied colonyof tree-nesting Great Cormorants did not follow thecentral-periphery model. Our results do not allow any cleardistinction between the satellite and the random models ofclutch-size distribution. The performed variogram analysissuggested satellite model at short lags; however, distribution

Fig. 2. Small-scale standardized variograms for laying date (a),clutch size (b), and fledging success (c) of Great Cormorants (Pha-lacrocorax carbo sinensis) at the Jeziorsko reservoir, central Poland.Semivariances are shown in three chosen lags, with high values in-dicating negative autocorrelation and a low value indicating a posi-tive autocorrelation. Broken horizontal line indicates standardizedtotal variance. Number of pair comparisons given in each case.

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across the whole colony was found to be random. In manyavian studies, clutch size was proposed to be a reliable indexof female quality (Slagsvold and Lifjeld 1990). Numerousstudies confirmed a positive influence of female condition(Bolton et al. 1993) and age (Hamann and Cooke 1987; Blaset al. 2009) on clutch size. Under the assumption that distri-bution of clutch size reliably reflects distribution of pair qual-ity, the random or satellite model indicates that the habitatwithin colonies of tree-nesting waterbirds may produce suffi-ciently high variation in nesting-site quality to disrupt thecentral-periphery gradients. This indicates that high-qualitypairs are likely to occupy attractive nesting sites irrespec-tively of their location within the colony. There are several

studies that report relationships between nest-site characteris-tics and reproductive output in tree-nesting waterbirds. Nestsurvival of White Ibis (Eudocimus albus (L., 1758)) corre-lated with nest stability and nest height, which reflected easeof access to predators (Post 1990). Olmos (2003) found pos-itive correlations between breeding success and nest cover byoverhanging branches in Scarlet Ibis (Eudocimus ruber (L.,1758)). Hatching success of Cattle Egrets was related withnest height, although no relationship was found betweenclutch size and physical characteristics of nests (Ranglack etal. 1991). Another study on Cattle Egrets demonstratedhigher fledging success in the nests located close to the trunkof the trees, which could affect their stability (Si Bachir et al.2008). In Great Cormorant, the variation in the quality ofnesting sites is expected to depend on similar characteristics,mainly nest height and nest stability. Nests located high overthe ground level may be less accessible for ground-dwellingor tree-dwelling predators, while tree diameter and morpho-logical structure of tree crown are likely to affect nest stabil-ity and determine probability of nest collapse during the eggincubation or chick-rearing period. An additional advantageof nesting in a high position is increased visibility, whichpromotes successful escape of adult birds in the case of dan-ger (Bregnballe and Gregersen 2003). For these reasons, agood-quality nesting site located in the peripheral zones ofthe colony may provide greater safety for chicks and their pa-rents compared with the low-quality sites in the central zone.In fact, higher reproductive success of birds nesting high inthe canopy top has been reported in Great Cormorants breed-ing in Kenya (Childress and Bennun 2000). In this study, weconfirmed a positive relationship between clutch size andnest height, which suggested higher quality of birds occupy-ing nests located high off the ground. The correlation be-tween nest height and clutch size has been reported also fortree-nesting Double-crested Cormorants (Phalacrocorax auri-tus (Lesson, 1831)) (Blomme 1979).Although there was a strong support for the random pat-

tern of distribution of pair quality in the colony, the satellitemodel could not be excluded with certainty based on geostat-istical analysis. The satellite pattern in the pair-quality distri-bution could be explained with higher chances of achievingextra-pair copulations or taking a better nesting place in thefollowing years by poor-quality birds nesting close to high-quality conspecifics. It was shown in the European Shag thatmales vary more in reproductive success than females owingto the high rate of extra-pair paternity (EPP) achieved bygood-quality individuals (Graves et al. 1993). Pairs of Euro-pean Shag that had smaller broods at fledging were morelikely to have an extra-pair chick and EPP was confirmed in18% of all chicks (Graves et al. 1992). A similar level of EPPwas found in Great Cormorant, but in some populations of itsnominate subspecies, EPP was recorded even in 40% ofchicks (Piertney et al. 2003). There is an evidence that extra-pair copulations could entail a mate change (Ens et al. 1993)and acquisition of better mate would be highly beneficial interms of fitness for a poor-quality female. Assuming highvariation in nesting-site quality, an additional advantage ofclustering close to high-quality breeders is a higher chanceof taking the better site in the following years by poor-qualitypairs. It was found that the probability of interseasonalchanges of nesting sites within the colony of European Shag

Fig. 3. Large-scale standardized variograms for laying date (a),clutch size (b), and fledging success (c) of Great Cormorants (Pha-lacrocorax carbo sinensis) at the Jeziorsko reservoir, central Poland.Semivariances are shown in nine chosen lags, with high values indi-cating negative autocorrelation and a low value indicating a positiveautocorrelation. Broken horizontal line indicates standardized totalvariance. Number of pair comparisons given in each case.

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depended on the distance between the sites (Aebischer et al.1995).Contrary to our predictions, the distribution of fledging

success followed a clear central-periphery pattern within thestudied colony. Number of fledged chicks is known to de-pend on pair quality, which corresponds with parental rearingcapacities. There are several nonexclusive mechanisms inwhich parental quality expressed by age, social status, orphysical condition may affect chick survival and fledgingsuccess. Firstly, older parents are likely to maximize fitnessby exhibiting greater parental investment compared withyoung breeders (Trivers 1974). Parental investment is alsoknown to be dependent on the physical condition of bothmale and female (Erikstad et al. 1997). Lastly, chick survivaland fledging success depends on food-provisioning rate,which is likely to be related with experience and conditionof parents (van de Pol et al. 2006). Female quality may alsoaffect fledging success indirectly with the production of big-ger clutches. Nevertheless, in contrast to clutch size, fledgingsuccess is known to be affected not only by the intrinsicquality of females, but also by the level of predation rate, anadditional strong selective pressure. The magnitude ofpredation-related egg or chick losses may be considerable inwaterbird colonies. In the colony of Great Cormorants at theJeziorsko reservoir, 24.6% of breeding attempts were unsuc-cessful in 2004 (P. Minias, unpublished data). Disproportion-ally higher predation rate in the peripheral, less denselyoccupied parts of waterbird colonies compared with the cen-tral sites could explain the central-periphery gradient offledging success within the colony, regardless of clutch sizeand pair-quality distribution. We found that the effect of nestdensity on fledging success was much stronger than its rela-tionship with clutch size, which may be related with higherefficiency of group defence in the areas of dense nest aggre-gations. An incongruity in the spatial patterns of clutch sizeand fledging success within the studied colony of Great Cor-morants implicates that, at least in some cases, fitness bene-fits from nesting in high densities may exceed the advantagesof occupying a good-quality nest sites in the peripheral zoneof the colony, even if the choice of nesting sites depends ontheir physical quality. It also suggests that distribution of re-productive success may not reliably reflect the distribution ofbirds of different intrinsic quality within waterbird colonies,as was suggested by other authors (Velando and Freire 2001).

AcknowledgementsFieldwork was performed with permission of the Regional

Environmental Protection Directorate in Łódź. The study wassupported by grant from the Ministry of Science and HigherEducation (N N303 319940). We want to thank all partici-pants of fieldworks, especially Michalina Mikłos and MaciejRakowski. We also thank two anonymous reviewers for theirhelpful comments on the earlier drafts of the manuscript.

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